Freezing Tolerance in Plants Requires Lipid Remodeling at the Outer Chloroplast Membrane

Moellering, Eric R.; Muthan, Bagyalakshmi; Benning, Christoph

doi:10.1126/science.1191803

Cited by 423 publications

(400 citation statements)

References 28 publications

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“…Accumulation of TAGs in leaves has been reported in Arabidopsis under freezing temperature and involves SENSITIVE TO FREEZING2 (SFR2), which encodes a galactolipid remodeling enzyme contributing to TAG accumulation (Moellering et al, 2010). We did not detect a change in SFR2 transcript level in wheat (Supplemental Data Set 9).…”

Section: Rna-seq Analysis Of Wheat Transcriptomementioning

confidence: 62%

“…We did not detect a change in SFR2 transcript level in wheat (Supplemental Data Set 9). However, studies have shown that SFR2 activity is primarily regulated at the posttranslational level during freezing tolerance (Moellering et al, 2010). Five genes potentially involved in TAG breakdown including LIPASE1 (El-Kouhen et al, 2005), SUGAR-DEPENDENT1 (Eastmond, 2006), MPL1 (El- Kouhen et al, 2005), and two putative TAGLs were downregulated more than 2-fold.…”

Section: Rna-seq Analysis Of Wheat Transcriptomementioning

confidence: 99%

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Understanding the Biochemical Basis of Temperature-Induced Lipid Pathway Adjustments in Plants

et al. 2015

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Glycerolipid biosynthesis in plants proceeds through two major pathways compartmentalized in the chloroplast and the endoplasmic reticulum (ER). The involvement of glycerolipid pathway interactions in modulating membrane desaturation under temperature stress has been suggested but not fully explored. We profiled glycerolipid changes as well as transcript dynamics under suboptimal temperature conditions in three plant species that are distinctively different in the mode of lipid pathway interactions. In Arabidopsis thaliana, a 16:3 plant, the chloroplast pathway is upregulated in response to low temperature, whereas high temperature promotes the eukaryotic pathway. Operating under a similar mechanistic framework, Atriplex lentiformis at high temperature drastically increases the contribution of the eukaryotic pathway and correspondingly suppresses the prokaryotic pathway, resulting in the switch of lipid profile from 16:3 to 18:3. In wheat (Triticum aestivum), an 18:3 plant, low temperature also influences the channeling of glycerolipids from the ER to chloroplast. Evidence of differential trafficking of diacylglycerol moieties from the ER to chloroplast was uncovered in three plant species as another layer of metabolic adaptation under temperature stress. We propose a model that highlights the predominance and prevalence of lipid pathway interactions in temperature-induced lipid compositional changes.

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Section: Rna-seq Analysis Of Wheat Transcriptomementioning

confidence: 62%

Section: Rna-seq Analysis Of Wheat Transcriptomementioning

confidence: 99%

Understanding the Biochemical Basis of Temperature-Induced Lipid Pathway Adjustments in Plants

et al. 2015

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“…Interestingly, AZI1 is induced in roots after ISR-inducing bacteria colonization 54 . A common feature of different stress signalling pathways may be the remodelling of chloroplast OEM lipids as well as PM lipids and reactive oxygen species production 55,56 . Moreover, several HyPRPs from different plant species have been reported to have roles in abiotic stress tolerance 38,[57][58][59] .…”

Section: Resultsmentioning

confidence: 99%

Arabidopsis AZI1 family proteins mediate signal mobilization for systemic defence priming

et al. 2015

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Priming is a major mechanism behind the immunological 'memory' observed during two key plant systemic defences: systemic acquired resistance (SAR) and induced systemic resistance (ISR). Lipid-derived azelaic acid (AZA) is a mobile priming signal. Here, we show that the lipid transfer protein (LTP)-like AZI1 and its closest paralog EARLI1 are necessary for SAR, ISR and the systemic movement and uptake of AZA in Arabidopsis. Imaging and fractionation studies indicate that AZI1 and EARLI1 localize to expected places for lipid exchange/movement to occur. These are the ER/plasmodesmata, chloroplast outer envelopes and membrane contact sites between them. Furthermore, these LTP-like proteins form complexes and act at the site of SAR establishment. The plastid targeting of AZI1 and AZI1 paralogs occurs through a mechanism that may enable/facilitate their roles in signal mobilization.

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“…One such candidate protein is SENSITIVE TO FREEZING2 (SFR2). SFR2 converts MGDG to DGDG and oligogalactolipids by transglycosylation with a concomitant production of DAG, which can be further metabolized to TAG (Moellering et al, 2010). The tgd1-1 mutant accumulates oligogalactolipids in leaves, indicating that SFR2 is activated in this mutant (Xu et al, 2003(Xu et al, , 2008Awai et al, 2006).…”

Section: Disruption Of Sensitive To Freezing2 Affects Lipid Content Amentioning

confidence: 99%

Arabidopsis Lipins, PDAT1 Acyltransferase, and SDP1 Triacylglycerol Lipase Synergistically Direct Fatty Acids toward β-Oxidation, Thereby Maintaining Membrane Lipid Homeostasis

et al. 2014

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Triacylglycerol (TAG) metabolism is a key aspect of intracellular lipid homeostasis in yeast and mammals, but its role in vegetative tissues of plants remains poorly defined. We previously reported that PHOSPHOLIPID:DIACYLGLYCEROL ACYLTRANSFERASE1 (PDAT1) is crucial for diverting fatty acids (FAs) from membrane lipid synthesis to TAG and thereby protecting against FA-induced cell death in leaves. Here, we show that overexpression of PDAT1 enhances the turnover of FAs in leaf lipids. Using the trigalactosyldiacylglycerol1-1 (tgd1-1) mutant, which displays substantially enhanced PDAT1-mediated TAG synthesis, we demonstrate that disruption of SUGAR-DEPENDENT1 (SDP1) TAG lipase or PEROXISOMAL TRANSPORTER1 (PXA1) severely decreases FA turnover, leading to increases in leaf TAG accumulation, to 9% of dry weight, and in total leaf lipid, by 3-fold. The membrane lipid composition of tgd1-1 sdp1-4 and tgd1-1 pxa1-2 double mutants is altered, and their growth and development are compromised. We also show that two Arabidopsis thaliana lipin homologs provide most of the diacylglycerol for TAG synthesis and that loss of their functions markedly reduces TAG content, but with only minor impact on eukaryotic galactolipid synthesis. Collectively, these results show that Arabidopsis lipins, along with PDAT1 and SDP1, function synergistically in directing FAs toward peroxisomal b-oxidation via TAG intermediates, thereby maintaining membrane lipid homeostasis in leaves.

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Freezing Tolerance in Plants Requires Lipid Remodeling at the Outer Chloroplast Membrane

Cited by 423 publications

References 28 publications

Understanding the Biochemical Basis of Temperature-Induced Lipid Pathway Adjustments in Plants

Understanding the Biochemical Basis of Temperature-Induced Lipid Pathway Adjustments in Plants

Arabidopsis AZI1 family proteins mediate signal mobilization for systemic defence priming

Arabidopsis Lipins, PDAT1 Acyltransferase, and SDP1 Triacylglycerol Lipase Synergistically Direct Fatty Acids toward β-Oxidation, Thereby Maintaining Membrane Lipid Homeostasis

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